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Unveiling the dynamic interplay between the hub- and spoke-components of the brain's semantic system and its impact on human behaviour.

ABSTRACT: The neural architecture of semantic knowledge comprises two key structures: (i) A set of widely dispersed regions, located adjacent to the sensorimotor cortices, serve as spokes that represent various modality-specific and context-dependent contents. (ii) The anterior-temporal lobe (ATL) serves as a hub that computes the nonlinear mappings required to transform modality-specific information into pan-modality, multifaceted concepts. Little is understood regarding whether neural dynamics between the hub and spokes might flexibly alter depending on the nature of a concept and how it impinges upon behaviour. Using fMRI, we demonstrate for the first time that the ATL serves as a 'pivot' which dynamically forms flexible long-range networks with cortical modules specialised for different domains (in the present case, the knowledge about actions and places). In two experiments, we manipulated semantic congruity and asked participants to recognise visually presented items. In Experiment 1 (dual-object displays), the ATL increased its functional coupling with the bilateral frontoparietal action-sensitive system when the objects formed a pair that permitted semantically meaningful action. In Experiment 2 (objects embedded in a scene), the ATL augmented its coupling with the retrosplenial cortex of the place-sensitive system when the objects and scene formed a semantically coherent ensemble. Causative connectivity revealed that, while communication between the hub and spokes was bidirectional, the hub's directional impact on spokes dwarfed the strength of the inverse spoke-to-hub connectivity. Furthermore, the size of behavioural congruity effects co-varied with the strength of neural coupling between the ATL hub and action- / place-related spokes, evident both at the within-individual level (the behavioural fluctuation across scanning runs) and between-individual level (the behavioural variation of between participants). Together, these findings have important implications for understanding the machinery that links neural dynamics with semantic cognition.

SUBMITTER: Chiou R

PROVIDER: S-EPMC6693526 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Unveiling the dynamic interplay between the hub- and spoke-components of the brain's semantic system and its impact on human behaviour.

Chiou Rocco R Lambon Ralph Matthew A MA

NeuroImage 20190524

The neural architecture of semantic knowledge comprises two key structures: (i) A set of widely dispersed regions, located adjacent to the sensorimotor cortices, serve as spokes that represent various modality-specific and context-dependent contents. (ii) The anterior-temporal lobe (ATL) serves as a hub that computes the nonlinear mappings required to transform modality-specific information into pan-modality, multifaceted concepts. Little is understood regarding whether neural dynamics between t ...[more]

PMID: 31132452

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Project description:Built upon a wealth of neuroimaging, neurostimulation, and neuropsychology data, a recent proposal set forth a framework termed controlled semantic cognition (CSC) to account for how the brain underpins the ability to flexibly use semantic knowledge (Lambon Ralph et al., 2017; Nature Reviews Neuroscience). In CSC, the 'semantic control' system, underpinned predominantly by the prefrontal cortex, dynamically monitors and modulates the 'semantic representation' system that consists of a 'hub' (anterior temporal lobe, ATL) and multiple 'spokes' (modality-specific areas). CSC predicts that unfamiliar and exacting semantic tasks should intensify communication between the 'control' and 'representation' systems, relative to familiar and less taxing tasks. In the present study, we used functional magnetic resonance imaging (fMRI) to test this hypothesis. Participants paired unrelated concepts by canonical colours (a less accustomed task - e.g., pairing ketchup with fire-extinguishers due to both being red) or paired well-related concepts by semantic relationship (a typical task - e.g., ketchup is related to mustard). We found the 'control' system was more engaged by atypical than typical pairing. While both tasks activated the ATL 'hub', colour pairing additionally involved occipitotemporal 'spoke' regions abutting areas of hue perception. Furthermore, we uncovered a gradient along the ventral temporal cortex, transitioning from the caudal 'spoke' zones preferring canonical colour processing to the rostral 'hub' zones preferring semantic relationship. Functional connectivity also differed between the tasks: Compared with semantic pairing, colour pairing relied more upon the inferior frontal gyrus, a key node of the control system, driving enhanced connectivity with occipitotemporal 'spoke'. Together, our findings characterise the interaction within the neural architecture of semantic cognition - the control system dynamically heightens its connectivity with relevant components of the representation system, in response to different semantic contents and difficulty levels.

Project description:The hub-and-spoke semantic representation theory posits that semantic knowledge is processed in a neural network, which contains an amodal hub, the sensorimotor modality-specific regions, and the connections between them. The exact neural basis of the hub, regions and connectivity remains unclear. Semantic dementia could be an ideal lesion model to construct the semantic network as this disease presents both amodal and modality-specific semantic processing (e.g. colour) deficits. The goal of the present study was to identify, using an unbiased data-driven approach, the semantic hub and its general and modality-specific semantic white matter connections by investigating the relationship between the lesion degree of the network and the severity of semantic deficits in 33 patients with semantic dementia. Data of diffusion-weighted imaging and behavioural performance in processing knowledge of general semantic and six sensorimotor modalities (i.e. object form, colour, motion, sound, manipulation and function) were collected from each subject. Specifically, to identify the semantic hub, we mapped the white matter nodal degree value (a graph theoretical index) of the 90 regions in the automated anatomical labelling atlas with the general semantic abilities of the patients. Of the regions, only the left fusiform gyrus was identified as the hub because its structural connectivity strength (i.e. nodal degree value) could significantly predict the general semantic processing of the patients. To identify the general and modality-specific semantic connections of the semantic hub, we separately correlated the white matter integrity values of each tract connected with the left fusiform gyrus, with the performance for general semantic processing and each of six semantic modality processing. The results showed that the hub region worked in concert with nine other regions in the semantic memory network for general semantic processing. Moreover, the connection between the hub and the left calcarine was associated with colour-specific semantic processing. The observed effects could not be accounted for by potential confounding variables (e.g. total grey matter volume, regional grey matter volume and performance on non-semantic control tasks). Our findings refine the neuroanatomical structure of the semantic network and underline the critical role of the left fusiform gyrus and its connectivity in the network.

Project description:The American Stroke Association guidelines emphasized the need for further high-quality studies that assess agreement by radiologists and nonradiologists engaged in emergency telestroke assessments and decision-making. Therefore, the objective of this study was to determine the level of agreement of baseline brain CT scan interpretations of patients with acute stroke presenting to telestroke spoke hospitals between central reading committee neuroradiologists and each of 2 groups, spoke hospital radiologists and hub hospital vascular neurologists (telestrokologists).The Stroke Team Remote Evaluation Using a Digital Observation Camera Arizona trial was a prospective, urban single-hub, rural 2-spoke, randomized, blinded, controlled trial of a 2-way, site-independent, audiovisual telemedicine and teleradiology system designed for remote evaluation of adult patients with acute stroke versus telephone consultation to assess eligibility for treatment with intravenous thrombolysis. In the telemedicine arm, the subjects' CT scans were interpreted by the hub telestrokologist and in the telephone arm by the spoke radiologist. All subjects' CT scans were subsequently interpreted centrally, independently, and blindly by 2 hub neuroradiologists. The primary CT outcome was determination of a CT-based contraindication to thrombolytic treatment. Kappa statistics and exact agreement rates were used to analyze interobserver agreement.Fifty-four subjects underwent random assignment. The overall agreement for the presence of radiological contraindications to thrombolysis was excellent (0.91) and did not differ substantially between the hub telestrokologist to neuroradiologist and spoke radiologist to neuroradiologist (0.92 and 0.89, respectively).In the context of a telestroke network designed to assess patients with acute stroke syndromes, agreement over the presence or absence of radiological contraindications to thrombolysis was excellent whether the comparisons were between a telestrokologist and neuroradiologist or between spoke radiologist and neuroradiologist.URL: http://www.clinicaltrials.gov. Unique identifier: NCT00623350.

Project description:Background and purposeTelestroke networks support screening for patients with emergent large-vessel occlusions who are eligible for endovascular thrombectomy. Ideal triage processes within telestroke networks remain uncertain. We characterize the impact of implementing a routine spoke hospital CTA protocol in our integrated telestroke network on transfer and thrombectomy patterns.Materials and methodsA protocol-driven CTA process was introduced at 22 spoke hospitals in November 2017. We retrospectively identified prospectively collected patients who presented to a spoke hospital with National Institutes of Health Stroke Scale scores ≥6 between March 1, 2016 and March 1, 2017 (pre-CTA), and March 1, 2018 and March 1, 2019 (post-CTA). We describe the demographics, CTA utilization, spoke hospital retention rates, emergent large-vessel occlusion identification, and rates of endovascular thrombectomy.ResultsThere were 167 patients pre-CTA and 207 post-CTA. The rate of CTA at spoke hospitals increased from 15% to 70% (P < .001). Despite increased endovascular thrombectomy screening in the extended window, the overall rates of transfer out of spoke hospitals remained similar (56% versus 54%; P = .83). There was a nonsignificant increase in transfers to our hub hospital for endovascular thrombectomy (26% versus 35%; P = .12), but patients transferred >4.5 hours from last known well increased nearly 5-fold (7% versus 34%; P < .001). The rate of endovascular thrombectomy performed on patients transferred for possible endovascular thrombectomy more than doubled (22% versus 47%; P = .011).ConclusionsImplementation of CTA at spoke hospitals in our telestroke network was feasible and improved the efficiency of stroke triage. Rates of patients retained at spoke hospitals remained stable despite higher numbers of patients screened. Emergent large-vessel occlusion confirmation at the spoke hospital lead to a more than 2-fold increase in thrombectomy rates among transferred patients at the hub.

Dataset Information

Unveiling the dynamic interplay between the hub- and spoke-components of the brain's semantic system and its impact on human behaviour.

Publications

Unveiling the dynamic interplay between the hub- and spoke-components of the brain's semantic system and its impact on human behaviour.

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